Improved annotation of the insect vector of citrus greening disease: biocuration by a diverse genomics community

Saha, Surya; Hosmani, Prashant S.; Villalobos-Ayala, Krystal; Miller, Sherry; Shippy, Teresa D.; Flores, Mirella; Rosendale, Andrew J.; Cordola, Chris; Bell, Tracey; Mann, Hannah; DeAvila, Gabe; DeAvila, Daniel; Moore, Zachary; Buller, Kyle; Ciolkevich, Kathryn; Nandyal, Samantha; Mahoney, Robert; Voorhis, Joshua Van; Dunlevy, Megan E.; Farrow, David; Hunter, David; Morgan, Taylar; Shore, Kayla; Guzman, Victoria; Izsak, Allison; Dixon, Danielle E.; Cridge, Andrew G.; Cano, Liliana; Cao, Xiaolong; Jiang, Haobo; Li, Nan; Johnson, Shannon L.; Cantarel, Brandi L.; Richards, Stephen; English, Adam C.; Shatters, Robert G.; Childers, Christopher P.; Chen, Mei Ju; Hunter, Wayne B.; Cilia, Michelle; Mueller, Lukas A.; Muñoz-Torres, Monica; Nelson, David R.; Poelchau, Monica; Benoit, Joshua B.; Wiersma-Koch, Helen; D’Elia, Tom; Brown, Susan J.

doi:10.1093/database/baz035

Cited by 13 publications

(20 citation statements)

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“…The genome of Acyrthosiphon pisum has recently been sequenced and shown to lack genes in the IMD pathway [66], and the IMD pathway genes are also notably absent from the transcriptome of the related, potato psyllid, Bactericera cockerelli [67]. No transcripts or proteins mapping to the IMD pathway were identified in our ACP dataset, although the ACP genome sequencing data are fragmented and the annotation of the genome is not complete [6, 32]. A previous transcriptomics analysis of the ACP also reported no transcripts belonging to the IMD pathway [47].…”

Section: Discussionmentioning

confidence: 99%

“…The filtered reads were aligned with RSEM [30] and bowtie2([31] rsem-calculate-expression—paired-end—strand-specific—bowtie2—estimate-rspd) to the cDNA transcripts (ftp://ftp.citrusgreening.org/genomes/Diaphorina_citri/annotation/NCBI_GNOMON/NCBI%20Diaphorina%20citri%20Annotation%20Release%20100/i5k/rna.fa.gz) generated by the NCBI Eukaryotic Annotation Pipeline (https://www.ncbi.nlm.nih.gov/genome/annotation_euk/process/, https://www.ncbi.nlm.nih.gov/genome/annotation_euk/Diaphorina_citri/100/) run on the NCBI diaci1.1 genome (ftp://ftp.citrusgreening.org/genomes/Diaphorina_citri/genome/NCBI-DIACI_v1.1/121845_ref_Diaci_psyllid_genome_assembly_version_1.1_chrUn.fa.gz) [6, 32]. All transcripts that had less than one count per million in less than three replicates were also excluded from downstream analysis [33].…”

Section: Methodsmentioning

confidence: 99%

“…A draft genome sequence is available for the ACP in NCBI, although the quality is poor (contig N50 of 34.4kp and scaffold N50 of 109.8kb). Extensive efforts are being made to improve the quality of the genome, as well as its annotation using long-read sequencing and community-driven manual curation (https://citrusgreening.org/annotation/index)[6]. The ACP has three known bacterial endosymbionts: Candidatus Profftella armatura, Candidatus Carsonella ruddii, and Wolbachia [7, 8] as well as other internal, extracellular bacteria [9].…”

Section: Introductionmentioning

confidence: 99%

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Combining 'omics and microscopy to visualize interactions between the Asian citrus psyllid vector and the Huanglongbing pathogen Candidatus Liberibacter asiaticus in the insect gut

et al. 2017

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Huanglongbing, or citrus greening disease, is an economically devastating bacterial disease of citrus. It is associated with infection by the gram-negative bacterium Candidatus Liberibacter asiaticus (CLas). CLas is transmitted by Diaphorina citri, the Asian citrus psyllid (ACP). For insect transmission to occur, CLas must be ingested during feeding on infected phloem sap and cross the gut barrier to gain entry into the insect vector. To investigate the effects of CLas exposure at the gut-pathogen interface, we performed RNAseq and mass spectrometry-based proteomics to analyze the transcriptome and proteome, respectively, of ACP gut tissue. CLas exposure resulted in changes in pathways involving the TCA cycle, iron metabolism, insecticide resistance and the insect’s immune system. We identified 83 long non-coding RNAs that are responsive to CLas, two of which appear to be specific to the ACP. Proteomics analysis also enabled us to determine that Wolbachia, a symbiont of the ACP, undergoes proteome regulation when CLas is present. Fluorescent in situ hybridization (FISH) confirmed that Wolbachia and CLas inhabit the same ACP gut cells, but do not co-localize within those cells. Wolbachia cells are prevalent throughout the gut epithelial cell cytoplasm, and Wolbachia titer is more variable in the guts of CLas exposed insects. CLas is detected on the luminal membrane, in puncta within the gut epithelial cell cytoplasm, along actin filaments in the gut visceral muscles, and rarely, in association with gut cell nuclei. Our study provides a snapshot of how the psyllid gut copes with CLas exposure and provides information on pathways and proteins for targeted disruption of CLas-vector interactions at the gut interface.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Combining 'omics and microscopy to visualize interactions between the Asian citrus psyllid vector and the Huanglongbing pathogen Candidatus Liberibacter asiaticus in the insect gut

et al. 2017

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“…For example, M. musculus and A. rosae have two alternatively spliced isoforms (Shah et al ., ; Sekiné et al ., ), whereas three paralogous genes are reported in M. lignano (Kuales et al ., ). The sequenced genome and many transcriptomes of D. citri are available in NCBI (Hunter et al ., ; Reese et al ., ; Vyas et al ., ; Saha et al ., ). In the present study, two transcripts ( DcBol and DcBol‐1 ) are identified by blast searches.…”

Section: Discussionmentioning

confidence: 99%

Effect of silencing a boule homologue on the survival and reproduction of Asian citrus psyllid Diaphorina citri

Killiny

2018

Physiol. Entomol.

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The fertility gene boule is conserved in most organisms and deletion of boule is found to block meiosis during spermatogenesis, which contributes to male infertility. The biological role of boule in Asian citrus psyllid Diaphorina citri, currently the most serious citrus pest and the vector of huanglongbing (HLB) pathogen, remains poorly understood. In the present study, a boule homologue in Diaphorina citri (DcBol) is identified and the potential application of DcBol for RNA interference (RNAi) based control of D. citri is evaluated. DcBol is constitutively expressed at gonadal and somatic tissues in both sexes. DsDcBol appears to be refractory to the salivary proteins of D. citri and no degradation is discovered over a 3‐day feeding period. DsRNA‐mediated RNAi of DcBol is achieved via artificial feeding, with DsDcBol at 400 ng μL−1 being sufficient to knockdown endogenous DcBol expression. A further bioassay reveals that knockdown of DcBol causes higher mortality of adult D. citri. In comparison with the control, the number of eggs and offspring nymphs generated by RNAi males is not reduced significantly. The results of the present study indicate that DcBol may play a limited role in male fertility.

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“…Gene annotators can curate gene models based on evidence from mapped orthologs as well as transcriptomics and ab-initio gene predictions. The manual curations from Apollo are periodically exported and merged with the automatically annotated gene models which are then released to the community (Saha et al 2019). The platform has been used effectively for gene annotation by undergraduate students across multiple institutions and the curation workflow was described in Hosmani et al (Hosmani et al 2019).…”

Section: Gene-centric Databasementioning

confidence: 99%

Citrusgreening.org: An open access and integrated systems biology portal for the Huanglongbing (HLB) disease complex

Flores-Gonzalez

Hosmani

Fernandez-Pozo

et al. 2019

Preprint

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113

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We have created an open access web portal with pathosystem-wide resources and bioinformatics tools for the host citrus, the vector Asian citrus psyllid (ACP) and multiple pathogens including Ca. Liberibacter asiaticus. To the best of our knowledge, this is the first example of a database to use the pathosystem as a holistic framework to understand an insect transmitted plant disease. This endeavor integrates and enables the analysis of data sets generated by the community to study the citrus greening disease complex. Users can submit relevant data sets to enable sharing and allow the community to better analyze their data within an integrated system. The portal contains a variety of tools for omics data. Metabolic pathway databases, CitrusCyc and DiaphorinaCyc provide organism specific pathways that can be used to mine metabolomics, transcriptomics and proteomics results to identify pathways and regulatory mechanism involved in disease response. Psyllid Expression Network (PEN) contains expression profiles of ACP genes from multiple life stages, tissues, conditions and hosts. Citrus Expression Network (CEN) contains public expression data from multiple tissues and conditions for various citrus hosts. All tools like Apollo/JBrowse, Biocyc, Blast, CEN and PEN connect to a central database containing gene models for citrus, ACP and multiple Liberibacter pathogens. The portal also includes electrical penetration graph (EPG) recordings of ACP feeding on citrus, information about citrus rootstock trials and metabolomics data in addition to traditional omics data types with a goal of combining and mining all information related to a pathosystem. The portal includes user-friendly manual curation tools to allow the research community to continuously improve this knowledge base as more experimental research is published. Bulk downloads are available for all genome and annotation datasets from the FTP site (ftp://ftp.citrusgreening.org). The portal can be accessed at https://citrusgreening.org/.

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Improved annotation of the insect vector of citrus greening disease: biocuration by a diverse genomics community

Cited by 13 publications

References 0 publications

Combining 'omics and microscopy to visualize interactions between the Asian citrus psyllid vector and the Huanglongbing pathogen Candidatus Liberibacter asiaticus in the insect gut

Combining 'omics and microscopy to visualize interactions between the Asian citrus psyllid vector and the Huanglongbing pathogen Candidatus Liberibacter asiaticus in the insect gut

Effect of silencing a boule homologue on the survival and reproduction of Asian citrus psyllid Diaphorina citri

Citrusgreening.org: An open access and integrated systems biology portal for the Huanglongbing (HLB) disease complex

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